Direct Interactions of OCA-B and TFII-I Regulate Immunoglobulin Heavy-Chain Gene Transcription by Facilitating Enhancer-Promoter Communication

Molecular Cell

Volumn 42, Issue 3, 2011, Pages 342-355

  Ren, Xiaodi ^a   Siegel, Rachael ^a   Kim, Unkyu ^a   Roeder, Robert G ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEACETYLASE 3; TRANSCRIPTION FACTOR PAX5;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; IMMUNOGLOBULIN HEAVY CHAIN GENE; IN VIVO STUDY; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; REGULATORY MECHANISM;

ANIMALS; B-LYMPHOCYTES; BASE SEQUENCE; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; ENHANCER ELEMENTS, GENETIC; HISTONE DEACETYLASES; HUMANS; IMMUNOBLOTTING; IMMUNOGLOBULIN HEAVY CHAINS; MICE; MODELS, GENETIC; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REPETITIVE SEQUENCES, NUCLEIC ACID; RNA INTERFERENCE; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS, TFII; TRANSCRIPTION, GENETIC;

EID: 79955504221     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2011.04.011     Document Type: Article

References (59)

1. Bebin A.G., Carrion C., Marquet M., Cogne N., Lecardeur S., Cogne M., Pinaud E. In vivo redundant function of the 3' IgH regulatory element HS3b in the mouse. J. Immunol. 2010, 184:3710-3717.
2. Bertolino E., Singh H. POU/TBP cooperativity: a mechanism for enhancer action from a distance. Mol. Cell 2002, 10:397-407.
3. Bulger M., Groudine M. Looping versus linking: toward a model for long-distance gene activation. Genes Dev. 1999, 13:2465-2477.
4. Calame K., Sen R. Transcription of immunoglobulin genes. Molecular Biology of B Cells 2003, 79-96. Elsevier Science Publishing Co. Inc., New York. F.A.T. Honjo, M. Neuberger (Eds.).
5. Carter D., Chakalova L., Osborne C.S., Dai Y.F., Fraser P. Long-range chromatin regulatory interactions in vivo. Nat. Genet. 2002, 32:623-626.
6. Cepek K.L., Chasman D.I., Sharp P.A. Sequence-specific DNA binding of the B-cell-specific coactivator OCA-B. Genes Dev. 1996, 10:2079-2088.
7. Corcoran L.M., Hasbold J., Dietrich W., Hawkins E., Kallies A., Nutt S.L., Tarlinton D.M., Matthias P., Hodgkin P.D. Differential requirement for OBF-1 during antibody-secreting cell differentiation. J. Exp. Med. 2005, 201:1385-1396.
8. Dekker J., Rippe K., Dekker M., Kleckner N. Capturing chromosome conformation. Science 2002, 295:1306-1311.
9. Dunnick W.A., Shi J., Graves K.A., Collins J.T. The 3' end of the heavy chain constant region locus enhances germline transcription and switch recombination of the four gamma genes. J. Exp. Med. 2005, 201:1459-1466.
10. Gilmore G.L., Yang J.Q., Marcu K.B., Birshtein B.K. Absence of somatic mutation in the variable region of MPC 11 variants expressing a different heavy chain isotype. J. Immunol. 1987, 139:619-624.
11. Gregor P.D., Kobrin B.J., Milcarek C., Morrison S.L. Sequences 3' of immunoglobulin heavy chain genes influence their expression. Immunol. Rev. 1986, 89:31-48.
12. Gstaiger M., Knoepfel L., Georgiev O., Schaffner W., Hovens C.M. A B-cell coactivator of octamer-binding transcription factors. Nature 1995, 373:360-362.
13. Gstaiger M., Georgiev O., van Leeuwen H., van der Vliet P., Schaffner W. The B cell coactivator Bob1 shows DNA sequence-dependent complex formation with Oct-1/Oct-2 factors, leading to differential promoter activation. EMBO J. 1996, 15:2781-2790.
14. Hagege H., Klous P., Braem C., Splinter E., Dekker J., Cathala G., de Laat W., Forne T. Quantitative analysis of chromosome conformation capture assays (3C-qPCR). Nat. Protoc. 2007, 2:1722-1733.
15. Hess J., Nielsen P.J., Fischer K.D., Bujard H., Wirth T. The B lymphocyte-specific coactivator BOB.1/OBF.1 is required at multiple stages of B-cell development. Mol. Cell. Biol. 2001, 21:1531-1539.
16. Jacob J., Przylepa J., Miller C., Kelsoe G. In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. III. The kinetics of V region mutation and selection in germinal center B cells. J. Exp. Med. 1993, 178:1293-1307.
17. Jenuwein T., Grosschedl R. Complex pattern of immunoglobulin mu gene expression in normal and transgenic mice: nonoverlapping regulatory sequences govern distinct tissue specificities. Genes Dev. 1991, 5:932-943.
18. Johnston C.M., Wood A.L., Bolland D.J., Corcoran A.E. Complete sequence assembly and characterization of the C57BL/6 mouse Ig heavy chain V region. J. Immunol. 2006, 176:4221-4234.
19. Ju Z., Volpi S.A., Hassan R., Martinez N., Giannini S.L., Gold T., Birshtein B.K. Evidence for physical interaction between the immunoglobulin heavy chain variable region and the 3' regulatory region. J. Biol. Chem. 2007, 282:35169-35178.
20. Khamlichi A.A., Pinaud E., Decourt C., Chauveau C., Cogne M. The 3' IgH regulatory region: a complex structure in a search for a function. Adv. Immunol. 2000, 75:317-345.
21. Kim U., Qin X.F., Gong S., Stevens S., Luo Y., Nussenzweig M., Roeder R.G. The B-cell-specific transcription coactivator OCA-B/OBF-1/Bob-1 is essential for normal production of immunoglobulin isotypes. Nature 1996, 383:542-547.
22. Kim U., Siegel R., Ren X., Gunther C.S., Gaasterland T., Roeder R.G. Identification of transcription coactivator OCA-B-dependent genes involved in antigen-dependent B cell differentiation by cDNA array analyses. Proc. Natl. Acad. Sci. USA 2003, 100:8868-8873.
23. Lieberman-Aiden E., van Berkum N.L., Williams L., Imakaev M., Ragoczy T., Telling A., Amit I., Lajoie B.R., Sabo P.J., Dorschner M.O., et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 2009, 326:289-293.
24. Liu Z., Garrard W.T. Long-range interactions between three transcriptional enhancers, active Vkappa gene promoters, and a 3' boundary sequence spanning 46 kilobases. Mol. Cell. Biol. 2005, 25:3220-3231.
25. Luo Y., Roeder R.G. Cloning, functional characterization, and mechanism of action of the B-cell-specific transcriptional coactivator OCA-B. Mol. Cell. Biol. 1995, 15:4115-4124.
26. Luo Y., Fujii H., Gerster T., Roeder R.G. A novel B cell-derived coactivator potentiates the activation of immunoglobulin promoters by octamer-binding transcription factors. Cell 1992, 71:231-241.
27. Madisen L., Groudine M. Identification of a locus control region in the immunoglobulin heavy-chain locus that deregulates c-myc expression in plasmacytoma and Burkitt's lymphoma cells. Genes Dev. 1994, 8:2212-2226.
28. Manis J.P., van der Stoep N., Tian M., Ferrini R., Davidson L., Bottaro A., Alt F.W. Class switching in B cells lacking 3' immunoglobulin heavy chain enhancers. J. Exp. Med. 1998, 188:1421-1431.
29. Matthias P. Lymphoid-specific transcription mediated by the conserved octamer site: who is doing what?. Semin. Immunol. 1998, 10:155-163.
30. McHeyzer-Williams M.G., McLean M.J., Lalor P.A., Nossal G.J. Antigen-driven B cell differentiation in vivo. J. Exp. Med. 1993, 178:295-307.
31. Michaelson J.S., Giannini S.L., Birshtein B.K. Identification of 3' alpha-hs4, a novel Ig heavy chain enhancer element regulated at multiple stages of B cell differentiation. Nucleic Acids Res. 1995, 23:975-981.
32. Nielsen P.J., Georgiev O., Lorenz B., Schaffner W. B lymphocytes are impaired in mice lacking the transcriptional co-activator Bob1/OCA-B/OBF1. Eur. J. Immunol. 1996, 26:3214-3218.
33. Novina C.D., Cheriyath V., Roy A.L. Regulation of TFII-I activity by phosphorylation. J. Biol. Chem. 1998, 273:33443-33448.
34. Novina C.D., Kumar S., Bajpai U., Cheriyath V., Zhang K., Pillai S., Wortis H.H., Roy A.L. Regulation of nuclear localization and transcriptional activity of TFII-I by Bruton's tyrosine kinase. Mol. Cell. Biol. 1999, 19:5014-5024.
35. Pinaud E., Khamlichi A.A., Le Morvan C., Drouet M., Nalesso V., Le Bert M., Cogne M. Localization of the 3' IgH locus elements that effect long-distance regulation of class switch recombination. Immunity 2001, 15:187-199.
36. Roy A.L. Signal-induced functions of the transcription factor TFII-I. Biochim. Biophys. Acta 2007, 1769:613-621.
37. Roy A.L., Meisterernst M., Pognonec P., Roeder R.G. Cooperative interaction of an initiator-binding transcription initiation factor and the helix-loop-helix activator USF. Nature 1991, 354:245-248.
38. Roy A.L., Du H., Gregor P.D., Novina C.D., Martinez E., Roeder R.G. Cloning of an inr- and E-box-binding protein, TFII-I, that interacts physically and functionally with USF1. EMBO J. 1997, 16:7091-7104.
39. Sacristan C., Tussie-Luna M.I., Logan S.M., Roy A.L. Mechanism of Bruton's tyrosine kinase-mediated recruitment and regulation of TFII-I. J. Biol. Chem. 2004, 279:7147-7158.
40. Samardzic T., Marinkovic D., Nielsen P.J., Nitschke L., Wirth T. BOB.1/OBF.1 deficiency affects marginal-zone B-cell compartment. Mol. Cell. Biol. 2002, 22:8320-8331.
41. Schubart D.B., Rolink A., Kosco-Vilbois M.H., Botteri F., Matthias P. B-cell-specific coactivator OBF-1/OCA-B/Bob1 required for immune response and germinal centre formation. Nature 1996, 383:538-542.
42. Schubart D.B., Rolink A., Schubart K., Matthias P. Cutting edge: lack of peripheral B cells and severe agammaglobulinemia in mice simultaneously lacking Bruton's tyrosine kinase and the B cell-specific transcriptional coactivator OBF-1. J. Immunol. 2000, 164:18-22.
43. Shen Y., Hendershot L.M. Identification of ERdj3 and OBF-1/BOB-1/OCA-B as direct targets of XBP-1 during plasma cell differentiation. J. Immunol. 2007, 179:2969-2978.
44. Shi X., Eckhardt L.A. Deletional analyses reveal an essential role for the hs3b/hs4 IgH 3' enhancer pair in an Ig-secreting but not an earlier-stage B cell line. Int. Immunol. 2001, 13:1003-1012.
45. Spilianakis C.G., Lalioti M.D., Town T., Lee G.R., Flavell R.A. Interchromosomal associations between alternatively expressed loci. Nature 2005, 435:637-645.
46. Staudt L.M., Lenardo M.J. Immunoglobulin gene transcription. Annu. Rev. Immunol. 1991, 9:373-398.
47. Stevens S., Ong J., Kim U., Eckhardt L.A., Roeder R.G. Role of OCA-B in 3'-IgH enhancer function. J. Immunol. 2000, 164:5306-5312.
48. Strubin M., Newell J.W., Matthias P. OBF-1, a novel B cell-specific coactivator that stimulates immunoglobulin promoter activity through association with octamer-binding proteins. Cell 1995, 80:497-506.
49. Tang H., Sharp P.A. Transcriptional regulation of the murine 3' IgH enhancer by OCT-2. Immunity 1999, 11:517-526.
50. Tantin D., Tussie-Luna M.I., Roy A.L., Sharp P.A. Regulation of immunoglobulin promoter activity by TFII-I class transcription factors. J. Biol. Chem. 2004, 279:5460-5469.
51. Tolhuis B., Palstra R.J., Splinter E., Grosveld F., de Laat W. Looping and interaction between hypersensitive sites in the active beta-globin locus. Mol. Cell 2002, 10:1453-1465.
52. Tsukada S., Rawlings D.J., Witte O.N. Role of Bruton's tyrosine kinase in immunodeficiency. Curr. Opin. Immunol. 1994, 6:623-630.
53. Tussie-Luna M.I., Bayarsaihan D., Seto E., Ruddle F.H., Roy A.L. Physical and functional interactions of histone deacetylase 3 with TFII-I family proteins and PIASxbeta. Proc. Natl. Acad. Sci. USA 2002, 99:12807-12812.
54. Vakoc C.R., Letting D.L., Gheldof N., Sawado T., Bender M.A., Groudine M., Weiss M.J., Dekker J., Blobel G.A. Proximity among distant regulatory elements at the beta-globin locus requires GATA-1 and FOG-1. Mol. Cell 2005, 17:453-462.
55. Vincent-Fabert C., Truffinet V., Fiancette R., Cogne N., Cogne M., Denizot Y. Ig synthesis and class switching do not require the presence of the hs4 enhancer in the 3' IgH regulatory region. J. Immunol. 2009, 182:6926-6932.
56. Vincent-Fabert C., Fiancette R., Pinaud E., Truffinet V., Cogne N., Cogne M., Denizot Y. Genomic deletion of the whole IgH 3' regulatory region (hs3a, hs1,2, hs3b, hs4) dramatically affects class switch recombination and Ig secretion to all isotypes. Blood 2010, 116:1895-1898.
57. Wen Y.D., Cress W.D., Roy A.L., Seto E. Histone deacetylase 3 binds to and regulates the multifunctional transcription factor TFII-I. J. Biol. Chem. 2003, 278:1841-1847.
58. Wirth T., Staudt L., Baltimore D. An octamer oligonucleotide upstream of a TATA motif is sufficient for lymphoid-specific promoter activity. Nature 1987, 329:174-178.
59. Yang W., Desiderio S. BAP-135, a target for Bruton's tyrosine kinase in response to B cell receptor engagement. Proc. Natl. Acad. Sci. USA 1997, 94:604-609.